Singlet oxygen, a neglected but important environmental factor: Short-term and long-term effects on bacterioplankton composition in a humic lake

Environmental Microbiology

Volumn 12, Issue 12, 2010, Pages 3124-3136

  Glaeser, Stefanie P ^a   Grossart, Hans Peter ^b   Glaeser, Jens ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; FRESH WATER; RNA 16S; SINGLET OXYGEN;

ARTICLE; BACTERIUM; CHEMISTRY; CLASSIFICATION; DENATURING GRADIENT GEL ELECTROPHORESIS; ECOSYSTEM; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMIC SUBSTANCE; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; POPULATION DYNAMICS;

BACTERIA; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA, BACTERIAL; ECOSYSTEM; FRESH WATER; HUMIC SUBSTANCES; MOLECULAR SEQUENCE DATA; PHYLOGENY; POPULATION DYNAMICS; RNA, RIBOSOMAL, 16S; SINGLET OXYGEN; WATER MICROBIOLOGY;

ACIDIPHILIUM; ACTINOBACTERIA; ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA; NOVOSPHINGOBIUM; POLYNUCLEOBACTER NECESSARIUS;

EID: 78650038017     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2010.02285.x     Document Type: Article

References (79)

1. Allgaier, M., and Grossart, H.-P. (2006a) Diversity and seasonal dynamics of Actinobacteria populations in four lakes in northeastern Germany. Appl Environ Microbiol 72: 3489-3497.
2. Allgaier, M., and Grossart, H.-P. (2006b) Seasonal dynamics and phylogenetic diversity of free-living and particle-associated bacterial communities in four lakes in northeastern Germany. Aquat Microb Ecol 45: 115-128.
3. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
4. Anesio, A.M., and Granéli, W. (2003) Increased photoreactivity of DOC by acidification: implications for the carbon cycle in humic lakes. Limnol Oceanogr 48: 735-744.
5. Anesio, A.M., Granéli, W., Aiken, G.R., Kieber, D.J., and Mopper, K. (2005) Effect of humic substance photodegradation on bacterial growth and respiration in lake water. Appl Environ Microbiol 71: 6267-6275.
6. Basta, T., Buerger, S., and Stolz, A. (2005) Structural and replicative diversity of large plasmids from sphingomonads that degrade polycyclic aromatic compounds and xenobiotics. Microbiology 151: 2025-2037.
7. Baxter, R.M., and Carey, J.H. (1983) Evidence for photochemical generation of superoxide ion in humic waters. Nature 306: 575-576.
8. Bedulina, D.S., Timofeyev, M.A., Zimmer, M., Zwirnmann, E., Menzel, R., and Steinberg, C.E.W. (2010) Different natural organic matter isolates cause similar stress response patterns in the freshwater amphipod, Gammarus pulex. Environ Sci Pollut Res Int 17: 261-269.
9. Benner, R., and Biddanda, B. (1998) Photochemical transformations of surface and deep marine dissolved organic matter: effects on bacterial growth. Limnol Oceanogr 43: 1373-1378.
10. Bertilsson, S., and Tranvik, L.J. (2000) Photochemical transformation of dissolved organic matter in lakes. Limnol Oceanogr 45: 753-762.
11. Brinkhoff, T., and Muyzer, G. (1997) Increased species diversity and extended habitat range of sulphur-oxidizing Thiomicrospira spp. Appl Environ Microbiol 63: 3789-3796.
12. Briviba, K., Klotz, L.O., and Sies, H. (1997) Toxic and signaling effects of photochemically or chemically generated singlet oxygen in biological systems. Biol Chem 378: 1259-1265.
13. Buck, U., Grossart, H.P., Amann, R., and Pernthaler, J. (2009) Substrate incorporation patterns of bacterioplankton populations in stratified and mixed waters of a humic lake. Environ Microbiol 11: 1854-1865.
14. Burkert, U., Warnecke, F., Babenzien, D., Zwirnmann, E., and Pernthaler, J. (2003) Members of a readily enriched betaproteobacterial clade are common in surface waters of a humic lake. Appl Environ Microbiol 69: 6550-6559.
15. Cooper, W.J. (1989) Sunlight induced photochemistry of humic substances in natural waters: major reactive species. Adv Chem Ser 219: 332-362.
16. Crump, B.C., and Hobbie, J.E. (2005) Synchrony and seasonality in bacterioplankton communities of two temperate rivers. Limnol Oceanogr 50: 1718-1729.
17. Crump, B.C., Armbrust, E.V., and Baross, J.A. (1999) Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia river, its estuary, and the adjacent coastal ocean. Appl Environ Microbiol 65: 3192-3204.
18. Davies, M.J. (2005) The oxidative environment and protein damage. Biochim Biophys Acta 1703: 93-109.
19. DeRosa, M.C., and Crutchley, R.J. (2002) Photosensitized singlet oxygen and its applications. Coord Chem Rev 233-234: 351-371.
20. Dohrmann, A.B., and Tebbe, C.C. (2004) Microbial community analysis by PCR-single strand conformation polymorphism (PCR-SSCP). In Molecular Microbial Ecology Manual. Kowalchuk, G.A., De Bruijn, F.J., Head, I.M., Akkermans, A.D., and Van Elsas, J.D. (eds). Berlin, Germany: Springer, pp. 809-838.
21. Eichler, S., Weinbauer, M.G., Dominik, D., and Höfle, M.G. (2004) Extraction of total RNA and DNA from bacterioplankton. In Molecular Microbial Ecology Manual, 2nd edn. Kowalchuk, G.A., Bruijn, F.J.D., Head, I.M., Akkermans, A.D.L., and Van Elsas, J.D. (eds). Dordrecht, the Netherlands: Kluwer Academic Publishers, pp. 103-120.
22. Fuhrman, J.A. (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399: 541-548.
23. Geller, A. (1986) Comparison of mechanisms enhancing biodegradability of refractory lake water constituents. Limnol Oceanogr 31: 755-764.
24. Glaeser, J., and Klug, G. (2005) Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes. Microbiology 151: 1927-1938.
25. Glaeser, J., and Overmann, J. (1999) Selective enrichment and characterization of Roseospirillum parvum, gen. nov. and sp. nov., a new purple nonsulfur bacterium with unusual light absorption properties. Arch Microbiol 171: 405-416.
26. Glaeser, J., and Overmann, J. (2003) Characterization and in situ carbon metabolism of phototrophic consortia. Appl Environ Microbiol 69: 3739-3750.
27. Glaeser, S.P., Kampfer, P., Busse, H.-J., Langer, S., and Glaeser, J. (2009) Novosphingobium acidiphilum sp. nov., an acidophilic salt-sensitive bacterium isolated from the humic acid-rich Lake Grosse Fuchskuhle. Int J Syst Evol Microbiol 59: 323-330.
28. Glöckner, F.O., Zaichikov, E., Belkova, N., Denissova, L., Pernthaler, J., Pernthaler, A., and Amann, R. (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of Actinobacteria. Appl Environ Microbiol 66: 5053-5065.
29. Grossart, H.P., Jezbera, J., Hornak, K., Hutalle, K.M.L., Buck, U., and Simek, K. (2008) Top-down and bottom-up induced shifts in bacterial abundance, production and community composition in an experimentally divided humic lake. Environ Microbiol 10: 635-652.
30. Haag, W.R., and Hoigne, J. (1986) Singlet oxygen in surface waters. 3. Photochemical formation and steady-state concentrations in various types of waters. Environ Sci Technol 20: 341-348.
31. Haag, W.R., Hoigne, J., Gassman, E., and Braun, A.M. (1984a) Singlet oxygen in surface waters - Part I: furfuryl alcohol as a trapping agent. Chemosphere 13: 631-640.
32. Haag, W.R., Hoigne, J., Gassman, E., and Braun, A.M. (1984b) Singlet oxygen in surface waters - Part II: quantum yields of its production by some natural humic materials as a function of wavelength. Chemosphere 13: 641-650.
33. Hahn, M.W., Lang, E., Brandt, U., Wu, Q.L., and Scheuerl, T. (2009) Emended description of the genus Polynucleobacter and the species Polynucleobacter necessarius and proposal of two subspecies, P. necessarius subsp. necessarius subsp. nov. and P. necessarius subsp. asymbioticus subsp. nov. Int J Syst Evol Microbiol 59: 2002-2009.
34. Harvey, G.R., Boran, D.A., Chesal, L.A., and Tokar, J.M. (1983) The structure of marine fulvic and humic acids. Mar Chem 12: 119-132.
35. Haukka, K., Heikkinen, E., Kairesalo, T., Karjalainen, H., and Sivonen, K. (2005) Effect of humic material on the bacterioplankton community composition in boreal lakes and mesocosms. Environ Microbiol 7: 620-630.
36. Humphrey, B., Kjelleberg, S., and Marshall, K.C. (1983) Responses of marine bacteria under starvation conditions at a solid-water interface. Appl Environ Microbiol 45: 43-47.
37. Hutalle-Schmelzer, K.M.L., Zwirnmann, E., Krüger, A., and Grossart, H.-P. (2010) Enrichment and cultivation of pelagic bacteria from a humic lake using phenol and humic matter additions. FEMS Microbiol Ecol 72: 58-73.
38. Janse, I., Bok, J., and Zwart, G. (2004) A simple remedy against artifactual double bands in denaturing gradient gel electrophoresis. J Microbiol Methods 57: 279-281.
39. Jørgensen, N.O.G., Tranvik, L., Edling, H., Granéli, W., and Lindell, M. (1998) Effects of sunlight on occurrence and bacterial turnover of specific carbon and nitrogen compounds in lake water. FEMS Microbiol Ecol 25: 217-227.
40. Judd, K.E., Crump, B.C., and Kling, G.W. (2007) Bacterial responses in activity and community composition to photo-oxidation of dissolved organic matter from soil and surface waters. Aquat Sci 69: 96-107.
41. Kasalicky, V., Jezbera, J., Simek, K., and Hahn, M.W. (2010) Limnohabitans planktonicus sp. nov., and Limnohabitans parvus sp. nov., two novel planktonic Betaproteobacteria isolated from a freshwater reservoir and emended description of the genus Limnohabitans. Int J Syst Evol Microbiol (in press): doi: 10.1099/ijs.0.018952-0.
42. Kasprzak, P. (1993) The use of an artificially divided bog lakes in food-web studies. Verh Internat Verein Limnol 25: 625-656.
43. Kieber, R.J., Hydro, L.H., and Seaton, P.J. (1997) Photooxidation of triglycerides and fatty acids in seawater: implication toward the formation of marine humic substances. Limnol Oceanogr 42: 1454-1462.
44. Kjelleberg, S., Humphrey, B.A., and Marshall, K.C. (1983) Initial phases of starvation and activity of bacteria at surfaces. Appl Environ Microbiol 46: 978-984.
45. Koschel, R. (1995) Manipulation of whole lake ecosystems and long-term limnological observations in the Brandenburg-Mecklenburg lake district, Germany. Int Revue Gesamte Hydrobiol 80: 507-518.
46. Langenheder, S., Sobek, S., and Tranvik, L.J. (2006) Changes in bacterial community composition along a solar radiation gradient in humic waters. Aquat Sci 68: 415-424.
47. Latch, D.E., and McNeill, K. (2006) Microheterogeneity of singlet oxygen distributions in irradiated humic acid solutions. Science 311: 1743-1747.
48. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, et al. (2004) ARB: a software environment for sequence data. Nucleic Acid Res 32: 1363-1371.
49. Lunau, M., Lemke, A., Walther, K., Martens-Habbena, W., and Simon, M. (2005) An improved method for counting bacteria from sediments and turbid environments by epifluorescence microscopy. Environ Microbiol 7: 961-968.
50. MacManus-Spencer, L.A., Latch, D.E., Kroncke, K.M., and McNeill, K. (2005) Stable dioxetane precursors as selective trap-and-trigger chemiluminescent probes for singlet oxygen. Anal Chem 77: 1200-1205.
51. Méthe, B.A., Hiorns, W.D., and Zehr, J.P. (1998) Contrasts between marine and freshwater bacterial community composition: analysis of communities in Lake George and six other Adirondack lakes. Limnol Oceanogr 43: 368-374.
52. Mopper, K., Zhou, X., Kieber, R.J., Kieber, D.J., Sikoeski, R.J., and Jones, R.D. (1991) Photochemical degradation of dissolved organic carbon and its impact on the oceanic carbon cycle. Nature 353: 60-62.
53. Muyzer, G., De Waal, E.C., and Uitterlinden, A.G. (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59: 695-700.
54. g)) in aqueous solution by specific chemical trapping with sodium 1, 3-cyclohexadiene-1, 4-diethanoate. J Photochem Photobiol B 39: 146-155.
55. Newton, R.J., Kent, A.D., Triplett, E.W., and McMahon, K.D. (2006) Microbial community dynamics in a humic lake: differential persistence of common freshwater phylotypes. Environ Microbiol 8: 956-970.
56. Obernosterer, I., Reitner, R., and Herndl, G.J. (1999) Contrasting effects of solar radiation on dissolved organic matter and its bioavailability to marine bacterioplankton. Limnol Oceanogr 44: 1645-1654.
57. Paul, A., Hackbarth, S., Vogt, R.D., Roeder, B., Burnison, B.K., and Steinberg, C.E.W. (2004) Photogeneration of singlet oxygen by humic substances: comparison of humic substances of aquatic and terrestrial origin. Photochem Photobiol Sci 3: 273-280.
58. Peplies, J., Kottmann, R., Ludwig, W., and Glockner, F.O. (2008) A standard operating procedure for phylogenetic inference (SOPPI) using (rRNA) marker genes. Syst Appl Microbiol 31: 251-257.
59. Pérez, M.T., and Sommaruga, R. (2007) Interactive effects of solar radiation and dissolved organic matter on bacterial activity and community structure. Environ Microbiol 9: 2200-2210.
60. Pernthaler, J. (2005) Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol 3: 537-546.
61. Piccini, C., Conde, D., Pernthaler, J., and Sommaruga, R. (2009) Alteration of chromophoric dissolved organic matter by solar UV radiation causes rapid changes in bacterial community composition. Photochem Photobiol Sci 8: 1321-1328.
62. Pomeroy, L.R. (1974) The ocean's food web: a changing paradigm. Bioscience 24: 499-504.
63. Pullin, M.J., Bertilsson, S., Goldstone, J.V., and Voelker, B.M. (2004) Effects of sunlight and hydroxyl radicals on dissolved organic matter: bacterial growth efficiency and production of carboxylic acids and other substances. Limnol Oceanogr 49: 2011-2022.
64. Reitner, B., Herndl, G.J., and Herzig, A. (1997) Role of ultraviolet-B radiation on photochemical and microbial oxygen consumption in a humic-rich shallow lake. Limnol Oceanogr 42: 950-960.
65. Sachse, A., Babenzien, D., Ginzel, G., Gelbrecht, J., and Steinberg, C.E.W. (2001) Characterization of dissolved organic carbon (DOC) in a dystrophic lake and an adjacent fen. Biochemistry 54: 279-296.
66. Scully, N.M., Cooper, W.J., and Tranvik, L.J. (2003) Photochemical effects on microbial activity in natural waters: the interaction of reactive oxygen species and dissolved organic matter. FEMS Microbiol Ecol 46: 353-357.
67. Simek, K., Hornak, K., Jezbera, J., Masin, M., Nedoma, J., Gasol, J.M., and Schauer, M. (2005) Influence of top-down and bottom-up manipulations on the R-BT065 subcluster of beta-proteobacteria, an abundant group in bacterioplankton of a freshwater reservoir. Appl Environ Microbiol 71: 2381-2390.
68. Steinberg, C.E.W., Kamara, S., Prokhotskaya, V.Y., Manusadžianas, L., Karasyova, T.A., Timofeyev, M.A., et al. (2006) Dissolved humic substances - ecological driving forces from the individual to the ecosystem level? Freshw Biol 51: 1189-1210.
69. Tarao, M., Jezbera, J., and Hahn, M.W. (2009) Involvement of cell surface structures in size-independent grazing resistance of freshwater actinobacteria. Appl Environ Microbiol 75: 4720-4726.
70. Tatsuzawa, H., Maruyama, T., Misawa, N., Fujimori, K., Hori, K., Sano, Y., et al. (1998) Inactivation of bacterial respiratory chain enzymes by singlet oxygen. FEBS Lett 439: 329-333.
71. Tranvik, L.J. (1988) Availability of dissolved organic-carbon for planktonic bacteria in oligotrophic lakes of differing humic content. Microb Ecol 16: 311-322.
72. Tranvik, L.J., and Bertilsson, S. (2001) Contrasting effects of solar UV radiation on dissolved organic sources for bacterial growth. Ecol Lett 4: 458-463.
73. Tranvik, L., and Kokalj, S. (1998) Decreased biodegradability of algal DOC due to interactive effects of UV radiation and humic matter. Aquat Microb Ecol 14: 301-307.
74. Valentine, R.L., and Zepp, R.G. (1993) Formation of carbon monoxide from the photodegration of terrestrial dissolved organic carbon in natural waters. Environ Sci Technol 27: 409-412.
75. Warnecke, F., Amann, R., and Pernthaler, J. (2004) Actinobacterial 16S rRNA genes from freshwater habitats cluster in four distinct lineages. Environ Microbiol 6: 242-253.
76. Watanabe, K., Komatsu, N., Ishii, Y., and Negishi, M. (2009) Effective isolation of bacterioplankton genus Polynucleobacter from freshwater environments grown on photochemically degraded dissolved organic matter. FEMS Microbiol Ecol 67: 57-68.
77. Zepp, R.G., Wolfe, N.L., Baughman, G.L., and Hollis, R.C. (1977) Singlet oxygen in natural waters. Nature 267: 421-423.
78. Zepp, R.G., Schlotzhauer, P.F., and Sink, R.M. (1985) Photosensitized transformations involving electronic energy transfer in natural waters: role of humic substances. Environ Sci Technol 19: 74-81.
79. Zwart, G., Crump, B.C., Kamst-van Agterveld, M.P., Hagen, F., and Han, S.-K. (2002) Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microb Ecol 28: 141-155.